Abstract
Main conclusion
Blue-light positive phototropism in roots is masked by gravity and revealed in conditions of microgravity. In addition, the magnitude of red-light positive phototropic curvature is correlated to the magnitude of gravity.
Due to their sessile nature, plants utilize environmental cues to grow and respond to their surroundings. Two of these cues, light and gravity, play a substantial role in plant orientation and directed growth movements (tropisms). However, very little is currently known about the interaction between light- (phototropic) and gravity (gravitropic)-mediated growth responses. Utilizing the European Modular Cultivation System on board the International Space Station, we investigated the interaction between phototropic and gravitropic responses in three Arabidopsis thaliana genotypes, Landsberg wild type, as well as mutants of phytochrome A and phytochrome B. Onboard centrifuges were used to create a fractional gravity gradient ranging from reduced gravity up to 1g. A novel positive blue-light phototropic response of roots was observed during conditions of microgravity, and this response was attenuated at 0.1g. In addition, a red-light pretreatment of plants enhanced the magnitude of positive phototropic curvature of roots in response to blue illumination. In addition, a positive phototropic response of roots was observed when exposed to red light, and a decrease in response was gradual and correlated with the increase in gravity. The positive red-light phototropic curvature of hypocotyls when exposed to red light was also confirmed. Both red-light and blue-light phototropic responses were also shown to be affected by directional light intensity. To our knowledge, this is the first characterization of a positive blue-light phototropic response in Arabidopsis roots, as well as the first description of the relationship between these phototropic responses in fractional or reduced gravities.
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Abbreviations
- EMCS:
-
European Modular Cultivation System
References
Benjamins R, Ampudia CSG, Hooykaas PJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630
Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389
Briggs WR (1964) Phototropism in higher plants. In: Giese AC (ed) Photophysiology: general principles; action of light on plants, vol 1. Academic Press, New York, London, pp 223–271
Briggs WR (2014) Phootropism: some history, some puzzles, and a look ahead. Plant Physiol 164:13–23
Brinckmann E (2005) ESA hardware for plant research on the International Space Station. Adv Space Res 36:1162–1166
Brinckmann E, Schiller P (2002) Experiments with small animals in BIOLAB and EMCS on the International Space Station. Adv Space Res 30:809–814
Brown BA, Jenkins GI (2008) UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiol 146:576–588
Bunsen R, Roscoe HE (1863) Photo-chemical researches, part V. On the direct measurement of the chemical action of sunlight. Philos Trans R Soc Lond 153:139–160
Chen R, Rosen E, Masson PH (1999) Gravitropism in higher plants. Plant Physiol 120:343–350
Christie JM, Salomon M, Nozue K, Wada M, Briggs WR (1999) LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci USA 96:8779–8783
Christie JM, Blackwood L, Petersen J, Sullivan S (2014) Plant flavoprotein photoreceptors. Plant Cell Physiol 56:401–413
Correll MJ, Kiss JZ (2002) Interactions between gravitropism and phototropism in plants. J Plant Growth Regul 21:89–101
Correll MJ, Kiss JZ (2005) The roles of phytochromes in elongation and gravitropism of roots. Plant Cell Physiol 46:317–323
Correll MJ, Coveney KM, Raines SV, Mullen JL, Hangarter RP, Kiss JZ (2003) Phytochromes play a role in phototropism and gravitropism in Arabidopsis roots. Adv Space Res 31:2203–2210
Correll MJ, Pyle TP, Millar KD, Sun Y, Yao J, Edelmann RE, Kiss JZ (2013) Transcriptome analyses of Arabidopsis thaliana seedlings grown in space: implications for gravity-responsive genes. Planta 238:519–533
Darwin C, Darwin F (1880) The power of movement in plants. John Murray, London
Gilroy S, Bethke PC, Jones RL (1993) Calcium homeostasis in plants. J Cell Sci 106:453–461
Goyal A, Szarzynska B, Fankhauser C (2013) Phototropism: at the crossroads of light-signaling pathways. Trends Plant Sci 18:393–401
Hopkins JA, Kiss JZ (2012) Phototropism and gravitropism in transgenic lines of Arabidopsis altered in the phytochrome pathway. Physiol Plant 145:461–473
Janoudi A, Poff KL (1990) A common fluence threshold for first positive and second positive phototropism in Arabidopsis thaliana. Plant Physiol 94:1605–1608
Kaufman PB, Song I, Pharis RP (1987) Gravity perception and response mechanism in graviresponding cereal grass shoots. In: Purohit SS (ed) Hormonal regulation of plant growth and development. Springer, Netherlands, pp 189–200
Kiss JZ (1994) Negative phototropism in young gametophytes of the fern Schizaea pusilla. Plant Cell Environ 17:1339–1343
Kiss JZ (2000) Mechanisms of the early phases of plant gravitropism. Crit Rev Plant Sci 19:551–573
Kiss JZ (2007) Where’s the water? Hydrotropism in plants. Proc Natl Acad Sci USA 104:4247–4248
Kiss JZ (2014) Plant biology in reduced gravity on the Moon and Mars. Plant Biol 16:12–17
Kiss JZ (2015) Conducting plant experiments in space. Methods Mol Biol 1309:255–283
Kiss JZ, Mullen JL, Correll MJ, Hangarter RP (2003) Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant Physiol 131:1411–1417
Kiss JZ, Kumar P, Millar KD, Edelmann RE, Correll MJ (2009) Operations of a spaceflight experiment to investigate plant tropisms. Adv Space Res 44:879–886
Kiss JZ, Millar KD, Edelmann RE (2012) Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station. Planta 236:635–645
Kiss JZ, Aanes G, Schiefloe M, Coelho LH, Millar KD, Edelmann RE (2014) Changes in operational procedures to improve spaceflight experiments in plant biology in the European Modular Cultivation System. Adv Space Res 53:818–827
Kumar NS, Stevens MHH, Kiss JZ (2008) Plastid movement in statocytes of the arg1 (altered response to gravity) mutant. Am J Bot 95:177–184
Kutschera U, Briggs WR (2012) Root phototropism: from dogma to the mechanism of blue light perception. Planta 235:443–452
Kutschera U, Briggs WR (2016) Phototropic solar tracking in sunflower plants: an integrative perspective. Ann Bot 117:1–8
Lariguet P, Fankhauser C (2004) Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J 40:826–834
Laxmi A, Pan J, Morsy M, Chen R (2008) Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS One 3:e1510
Li FW, Mathews S (2016) Evolutionary aspects of plant photoreceptors. J Plant Res 129:115–122
Liscum E, Askinosie SK, Leuchtman DL, Morrow J, Willenburg KT, Coats DR (2014) Phototropism: growing towards an understanding of plant movement. Plant Cell 26:38–55
López-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bögre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968
Mandoli DF, Briggs WR (1984) Fiber optics in plants. Sci Am 251:90–98
Millar KD, Kumar P, Correll MJ, Mullen JL, Hangarter RP, Edelmann RE, Kiss JZ (2010) A novel phototropic response to red light is revealed in microgravity. New Phytol 186:648–656
Mo M, Yokawa K, Wan Y, Baluška F (2015) How and why do root apices sense light under the soil surface?. Front Plant Sci 6:775. doi:10.3389/fpls.2015.00775
Molas ML, Kiss JZ (2008) PKS1 plays a role in red-light-based positive phototropism in roots. Plant Cell Environ 31:842–849
Moni A, Lee AY, Briggs W, Han IS (2015) The blue light receptor Phototropin 1 suppresses lateral root growth by controlling cell elongation. Plant Biol 17:34–40
Neef M, Ecke M, Hampp R (2015) Real-time recording of cytosolic calcium levels in Arabidopsis thaliana cell cultures during parabolic flights. Microgravity Sci Tec 27:305–312
Ovid (8 AD) (2008) Metamorphosis. Oxford University Press, Oxford
Poovaiah B, Reddy A, Leopold AC (1987) Calcium messenger system in plants. Crit Rev Plant Sci 6:47–103
Sakai T, Haga K (2012) Molecular genetic analysis of phototropism in Arabidopsis. Plant Cell Physiol 53:1517–1534
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974
Shih H-W, DePew CL, Miller ND, Monshausen GB (2015) The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Curr Biol 25:3119–3125
Silva-Navas J, Moreno-Risueno MA, Manzano C, Pallero-Baena M, Navarro-Neila S, Téllez-Robledo B, Garcia-Mina JM, Baigorri R, Gallego FJ, Pozo JC (2015) D-Root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J 84:244–255
Sullivan S, Hart JE, Rasch P, Walker CH, Christie JM (2016) Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis. Front Plant Sci 7:290. doi:10.3389/fpls.2014.00563
Tester M, Morris C (1987) The penetration of light through soil. Plant, Cell Environ 10:281–286
Toyota M, Furuichi T, Sokabe M, Tatsumi H (2013) Analyses of a gravistimulation-specific Ca2+ signature in Arabidopsis using parabolic flights. Plant Physiol 163:543–554
Vandenbrink JP, Kiss JZ (2016) Space, the final frontier: a critical review of recent experiments performed in microgravity. Plant Sci 243:115–119
Vandenbrink JP, Brown EA, Harmer SL, Blackman BK (2014a) Turning heads: the biology of solar tracking in sunflower. Plant Sci 224:20–26
Vandenbrink JP, Kiss JZ, Herranz R, Medina FJ (2014b) Light and gravity signals synergize in modulating plant development. Front Plant Sci 5:563. doi:10.3389/fpls.2014.00563
Wada M (2007) The fern as a model system to study photomorphogenesis. J Plant Res 120:3–16
Whippo C, Hangarter R (2004) Phytochrome modulation of blue-light-induced phototropism. Plant Cell Environ 27:1223–1228
Woolley JT, Stoller EW (1978) Light penetration and light-induced seed germination in soil. Plant Physiol 61:597–600
Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Löfke C, Teichmann T, Bielach A, Cannoot B (2011) Inositol trisphosphate-induced Ca 2+ signaling modulates auxin transport and PIN polarity. Dev Cell 20:855–866
Acknowledgments
Funding for this study was provided by NASA Grant NNX12A065G, and we would like to acknowledge the fine support of NASA’s Ames Research Center. In addition to NASA, we would like to thank the European Space Agency and the Norwegian User Support and Operations Center (N-USOC) for their support on this project. Finally, we would like to thank the astronauts on board the ISS for their support, without whom these experiments would not be possible.
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425_2016_2581_MOESM1_ESM.tif
Supplementary material 1 (TIFF 155 kb) Suppl. Fig. S1 Heat map of blue light illumination within an individual seedling cassette
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Supplementary material 2 (TIFF 149 kb) Suppl. Fig. S2 Heat map of red-light illumination within an individual seedling cassette
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Vandenbrink, J.P., Herranz, R., Medina, F.J. et al. A novel blue-light phototropic response is revealed in roots of Arabidopsis thaliana in microgravity. Planta 244, 1201–1215 (2016). https://doi.org/10.1007/s00425-016-2581-8
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DOI: https://doi.org/10.1007/s00425-016-2581-8